Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e51160, enero-diciembre 2024 (Publicado Ago. 21, 2024)

Phytoplankton from a brackish lagoon

in the central region of Veracruz, Mexico

Gloria Garduño Solórzano1; https://orcid.org/0000-0002-3318-0891

José Manuel González Fernández1; https://orcid.org/0000-0003-1178-5600

Saúl Aldair Fuentes Zuno1; https://orcid.org/0000-002-0811-1720

1. Facultad de Estudios Superiores Iztacala, Universidad Nacional Autónoma de México (UNAM), México;

ggs@unam.mx (*Correspondence), m.gonzalez@iztacala.unam.mx, aldair.1559@gmail.com

Received 30-I-2024. Corrected 09-IV-2024. Accepted 01-VIII-2024.

ABSTRACT

Introduction: The brackish lagoons are ecosystems with great diversity and possibilities for human use.

Therefore, the knowledge about phytoplankton needs to be improved to understand its real impact.

Objective: To relate the Mandinga’s Lagoon phytoplankton to the limnological conditions during the dry and

wet seasons.

Methods: The material was collected in three stations: Isla Conchas (ICO), Mandinga Chica (MCH) and Isla del

Amor (IA) during the dry (March 2018) and wet (September 2017 and 2018) seasons. The limnological analysis

included ten abiotic variables, and the phytoplankton was analyzed by the Utermöhl method. Data was analyzed

with the Shannon index (H´) and Canonical Correspondence Analysis (CCA).

Results: 136 species were identified: 68.4 % Heterokontophyta, 22.8 % Dinoflagellata, and 5.9 % Cyanobacteria;

with 40 euryhaline and 96 stenohaline. The most abundant species were: Bacillaria paxillifera, Chaetoceros

compressus, Coscinodiscus rothii, and Chaetoceros atlanticus. The highest abundance was in ICO (dry) and the

lowest in MCH (wet), with 307 x 103 and 76 x 103 cells/ml, respectively; the H´ ranged from 1.31 to 0.70 bits/

ind. The CCA showed a relationship between salinity and dissolved oxygen with C. rothii and Ceratoneis closte-

rium. The phosphates were associated with B. paxillifera, C. atlanticus, and Podosira stelligera. The nitrate, water

temperature and pH were related to Tripos hircus, T. furca, Diploneis bombus, and Merismopedia elegans. In con-

trast, Skeletonema costatum, Cocconeis scutelum, and Nitzschia bicapitata did not correlate with the limnological

variables.

Conclusions: The Mandinga’s Lagoon is a shallow, euryhaline and well-oxygenated ecosystem. The dominance

of diatoms and dinoflagellates was evidenced by their ability to survive in different salinities and temperatures. It

is recommended monitor phytoplankton, in particular Microcystis wesenbergii, B. quinquecornis, Pseudo-nitzschia

cf. pungens, and P. cf. pseudodelicatissima as they are harmful algae.

Key words: Bacillariophytina; Dinoflagellata; tropical Lagoon; Canonical Correspondence Analysis; new records.

RESUMEN

Fitoplancton de una laguna salobre en la región central de Veracruz, México

Introducción: Las lagunas salobres son ecosistemas de alta diversidad y con posibilidades para uso humano. Por

lo que es necesario mejorar el conocimiento del fitoplancton para entender su impacto real.

Objetivo: Relacionar el fitoplancton de la Laguna Mandinga con las condiciones limnológicas durante épocas

de secas y lluvias.

https://doi.org/10.15517/rev.biol.trop..v72i1.51160

AQUATIC ECOLOGY

2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e51160, enero-diciembre 2024 (Publicado Ago. 21, 2024)

INTRODUCTION

In coastal lagoons, the physical and chemi-

cal variables are influenced by tidal currents,

upwellings, and seasonal cycles, as well as by

the effect of topography, sediment, type of

vegetation, river discharge, the effect of wind-

induced mixing, and the system morphology

itself (Kjerfve & Magill, 1989; Millán et al.,

1982). This condition plays an essential role in

modifying the population structure of phyto-

plankton, which groups the microscopic pho-

tosynthesizing organisms that live suspended

in the photic zone. As we know, phytoplankton

is a vital component of marine ecosystems

since it produces approximately half of the

global net primary production (Contreras &

Warner, 2004).

Additionally, phytoplankton species are

good bioindicators of hydro-climatic and

anthropogenic changes, and some species can

produce Harmful Algal Bloom (HAB) under

certain environmental conditions. It causes

deleterious impacts on organisms coexisting

with them and human health, with negative

consequences on the socio-economic activities

of coastal communities (Cortés-Altamirano et

al., 2019). In Veracruz, the HAB date from

1984 when a contingency occurred in the

Alvarado, Tamiahua, Sontecomapan, and Port

of Veracruz due to B. quinquecornis (=Peri-

dinium quinquecorne), Ceratium furca var.

hircus, Cyclotella spp., Chaetoceros holsaticus,

Karenia brevis, Peridinium quinquecorne var.

trispiniferum, Pyrodinium bahamense var. baha-

mense, Prorocentrum cordatum, Skeletonema

spp., and T. furca (=Ceratium furca) (Aké-Cas-

tillo & Vázquez-Hurtado, 2008; Aké-Castillo

& Vázquez-Hurtado, 2011; Gómez-Aguirre &

Licea, 1998; Guerra-Martínez & Lara-Villa,

1996; Licea et al., 2004).

In the coastal lagoons of the Gulf of Mexico,

various studies have been carried out focusing

on listing and understanding the phytoplankton

ecology. In Lagartos Lagoon, Quintana Roo, 67

taxa were registered. The highest abundance

corresponded to Cyanobacteria, with about 80

% (Nava-Ruíz & Valadez, 2012). Furthermore,

in Terminos Lagoon, Campeche, Muciño-

Márquez et al. (2014) tested the composition

and abundance of the phytoplankton and its

relationship with some physical and chemi-

cal variables in the Pom-Atasta and Palizada

del Este Lagoon systems, registering 263 and

348 taxa, with a predominance of diatoms

and dinoflagellates, respectively. In different

coastal lagoons of Veracruz, 14 genera of Cya-

nobacteria have been registered (Okolodkov

& Blanco, 2011). The Bacillariophyta exhibit

Métodos: El material se recolectó en tres estaciones: Isla Conchas (ICO), Mandinga Chica (MCH) e Isla del Amor

(IA) en secas (marzo 2018) y lluvias (septiembre 2017 y 2018). El análisis limnológico incluyó diez variables

abióticas, además del fitoplancton mediante el método de Utermöhl. Los datos fueron analizados por el índice de

Shannon (H´) y Correspondencia Canónica (ACC).

Resultados: Análisis de 136 especies; 68.4 % Heterokontophyta, 22.8 % Dinoflagellata, 5.9 % Cyanobacteria; con

40 eurihalinas y 96 estenohalinas. Las especies más abundantes fueron: Bacillaria paxillifera, Chaetoceros com-

pressus, Coscinodiscus rothii y Chaetoceros atlanticus. La mayor abundancia se registró en ICO (secas) y la menor

en MCH (lluvias) con 307 x 103 y 76 x 103 cell/ml, respectivamente. El H´ osciló entre 1.31 y 0.70 bits/ind. El

CCA mostró una relación entre salinidad y oxígeno disuelto con C. rothii y Ceratoneis closterium. Los fosfatos se

asociaron con B. paxillifera, C. atlanticus y Podosira stelligera. Los nitratos, temperatura y pH se correlacionaron

con Tripos hircus, T. furca, Diploneis bombus y Merismopedia elegans. Mientras, Skeletonema costatum, Cocconeis

scutelum y Nitzschia bicapitata no presentaron correlación con las variables limnológicas.

Conclusiones: La Laguna Mandinga es un ecosistema somero, eurihalino y bien oxigenado. La dominancia de

diatomeas y dinoflagelados se evidenció por su capacidad para sobrevivir en diferentes concentraciones de sali-

nidad y temperatura. Sugerimos monitorear al fitoplancton por la presencia de Microcystis wesenbergii, B. quin-

quecornis, Pseudo-nitzschia cf. pungens y P. cf. pseudodelicatissima ya que pueden formar proliferaciones dañinas.

Palabras clave: Bacillariophytina; Dinoflagellata; lagunas costeras; análisis de correspondencia canónica; nuevos

registros.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e51160, enero-diciembre 2024 (Publicado Ago. 21, 2024)

high species richness in Coscinodiscus, Chaeto-

ceros, Nitzschia, Rhizosolenia, and Thalassiosira

(Krayesky et al., 2009). In the meantime, 32

species of Chlorophyta have been registered

in mixohaline coastal lagoons. Although they

are not very abundant, the Euglenophyta indi-

cates contamination. In Alvarado’s Lagoon, 18

taxa marine or mesohaline taxa were investi-

gated in phytoplankton (Margalef, 1975). In

the Tamiahua Lagoon, 39 Dinoflagellata have

been recorded; it is known that Chlorophyta,

Euglenophyta, and Chrysophyta are euryha-

line common, while eutrophic estuaries are

characterized by a high diversity of Cyano-

bacteria (Figueroa-Torres & Weiss-Martínez,

1999). Instead, in the Sontecomapan Lagoon,

the morphology and distribution of the genus

Skeletonema were analyzed (Aké-Castillo et

al., 1995). For Mandinga Lagoon, Contreras-

Espinosa et al. (1994) have recognized it as a

eutrophic lagoon. Barón-Campis et al. (2005)

reported the genera Lioloma, Navicula, Pleu-

rosigma, Pseudo-nitzschia, and Thalassionema.

Also, Salcedo-Garduño et al. (2019) studied

the influence of physicochemical parameters

on the distribution of 47 phytoplankton spe-

cies. The Mandinga Lagoon is a vital ecosystem

for its diversity and environmental services

that benefit human use. However, knowledge

about phytoplankton in this ecosystem must be

improved to understand its real impact. Thus,

the objective was to relate the phytoplankton

diversity of Mandinga Lagoon with the physi-

cal and chemical conditions during the dry and

wet seasons of 2017-2018, respectively.

MATERIALS AND METHODS

Study area: Mandinga’s Lagoon, Veracruz

is located between (18º 59’-19º 05’ N & 96º

02’-96º 07’ W), has an approximate length of

20 km and is composed of six interconnected

bodies of water: Estero del Conchal, Laguna

Larga, Estero de Horcones, Laguna de Man-

dinga Chica or Laguna Redonda, Estero de

Mandinga, and Laguna de Mandinga Grande

Fig. 1. A. Map of Mexico, B. Veracruz state, C. Study area, location of the sampling sites in the Mandinga Lagoon: IA, Isla del

Amor; MCH, Mandinga Chica, and ICO, Isla Conchas.

4Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e51160, enero-diciembre 2024 (Publicado Ago. 21, 2024)

(Fig. 1). It is a tropical environment with a

temperature of 23.6-29 °C, the salinity of 18-31

PSU, and pH of 7.2. The dissolved oxygen con-

centration varies from 1.7 to 9.4 mg/L; NO3 and

PO4 between 0.15- 0.6 mg/L and 0.082 to 0.153

mg/L, respectively. In addition to chlorophyll-a

of 0.12 to 0.17 mg/L (Salcedo-Garduño et al.,

2016). Concerning rainfall, the highest annual

average was in September (2018) with 270 mm,

and the lowest was in April (2017) with 17 mm

during the dry season (Weather Spark, s.f.).

Also, in the lagoon, there are various fishing

resources of great economic value; it is one of

the primary Crassostrea virginica oyster pro-

ducers in the Gulf of Mexico, as well as Crys-

tal shrimp (Penaeus sp.) and crab (Callinectes

similis). Such products constitute an essential

income source for the surrounding settlements

(Lango et al., 2013).

Collection of biological material: The

samples of biological material were collected

in the wet (September 2017 and 2018) and dry

(March 2018) seasons in three stations: Isla

Conchas (ICO), Mandinga Chica (MCH), and

Isla del Amor (IA), respectively (Fig. 1). At each

station, horizontal trawling was performed for

five minutes using a net with a mesh size of 20

µm. This material was divided into two equal

fractions: the first was kept in vivo at a tempera-

ture of 4 °C, and the other was preserved with

formaldehyde at a final concentration of 4 %

with sodium borate (Tomas, 1997). Addition-

ally, two 500 ml samples were taken in the first

20 cm of the water column; one of them was

preserved with Lugol acetate for quantification

by the Utermöhl method (Edler & Elbrächter,

2010), and the second was used to determine

the limnological variables (APHA et al., 2005).

Limnological variables: In each study sta-

tion, registrations were made in situ for the

following variables. A Brannan thermometer

was used for water temperature; pH was mea-

sured using a Cole Parmer potentiometer and

Digi-sense model; the transparency and depth

were measured using Secchi Disc and Speed-

tech USA, respectively. Dissolved oxygen con-

centration and total alkalinity were measured

using the Winkler technique and methyl orange

titration. The salinity and electrical conduc-

tivity were recorded using an Atago PAL-03S

Japan refractometer and a Hanna HI98312.

Finally, a Hach spectrophotometer model

DR2800 was used, and the test package for

orthophosphates using the molybdovanadate

method 8114 and nitrates cadmium-reduction

method 8153 (APHA et al., 2005). Chloro-

phyll-a quantification (mg/m³): A 50 ml water

sample was collected using the Strickland &

Parsons (1972) technique.

Processing of biological material: The

phytoplankton samples were analyzed using a

Leica light microscope. In order to study the

thecal plates of dinoflagellates, 0.2 % trypan

blue (Taylor, 1978). For clean diatoms, the

oxidative method was used Hasle & Fryxell

(1970) and was subsequently observed with

a scanning electron microscope (SEM JEOL

model JSM6380LV) according to Ferrario et al.

(1995). The works of Tomas (1997), Komárek &

Anagnostidis (1999), Komárek & Anagnostidis

(2002), and Okolodkov (2008) were used for

taxonomic determination based on the classi-

fication indicated in the algae database (Guiry

& Guiry, 2024). Finally, the new registrations

for the Gulf of Mexico coasts were based on

Krayesky et al. (2009), León-Tejera et al. (2009),

Steidinger et al. (2009), and Salcedo-Garduño

et al. (2019). The material was placed in the

herbarium IZTA 1910-1914 (Thiers, 2020).

Statistical analysis: The Shannon-Wiener

Diversity Index and the Olmstead-Tukey analy-

sis were also carried out (Sokal & Rohlf, 1981).

Also, to know the relationship between the

dominant and constant species with limnologi-

cal variables, a CCA was performed using the

Monte Carlo permutation test (9999 permuta-

tions, α = 0.05) in the CANOCO software for

Windows 4.5 (Ter-Braak & Smilauer, 2009).

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e51160, enero-diciembre 2024 (Publicado Ago. 21, 2024)

RESULTS

Physical, chemical, nutrient, and chlo-

rophyll-a variable: Water temperature ranged

from 21 to 29 °C and salinity from 0 to 32 PSU.

Water pH was slightly alkaline with 8.0-8.8,

and a well-oxygenated environment valued at

6.0-12 mg L-1. Chlorophyll-a, transparency and

depth were higher in the wet season (Table 1).

Phytoplankton of composition: Table 2

shows the specific richness of phytoplankton

in the study area exhibited 40 species of eury-

haline and 96 of stenohaline. The distribution

was different in each of the stations: 53 spe-

cies were recorded at ICO; in the MCH, there

were 64 species, and finally, in IA, 79 species

were recognized.

Table 1

Values of environmental variables registered during dry and wet seasons at the sampled sites in the Mandinga Lagoon.

Sites of sampling Station 1-ICO Station 2-MCH Station 3-IA

Interval Seasons Dry Wet Dry Wet Dry Wet

Environmental variables

1. Water temperature (°C) 29 22 27 21 28 21 21-29

2. Ionization potential (pH) 8.4 8.1 8.8 8.0 8.5 8.1 8.0-8.8

3. Dissolved oxigen (mg/L) 6.8 9.2 8.4 12 6 3.6 6-12

4. Alcalinity (mg/L CaCO3) 89 220 20 230 80 225 20-230

5. Conductivity (µS/cm) 31 36 40 37 20 45 31-45

6. Salinity (PSU) 0 0 32 32

25 25 0-32

7. Nitrate (mg/L) 1 0 1 0 0 0-1

8. Phosphate (mg/L) 1 2.2 1 1.1 0 0.1 0-2.2

9. Chlorophyll-a (mg/m³) 3.2 11 3 9.0 3 8.1 3-11

10. Transparency (cm) 43 80 28 100 60 200 28-200

11. Depth (cm) 52 98 28 126 100 420 28-420

Station1-ICO: Station 1-Isla Conchas; Station 2-MCH: Station 2-Mandinga Chica and Station 3-IA: Station 3-Isla del Amor.

Table 2

List of Taxa registered at the sampled sites in the Mandinga Lagoon.

Sites of sampling S1-ICO S2-MCH S3-IA

Salinity (PSU) mean values 0 PSU 32 PSU 25 PSU

Cyanobacteria

Anabaena sp. 100

Johannespbatistia sp. 010

Leptolyngbya gracilis (Lindstedt)Anagnostidis & Komárek 100

Lyngbya sp. 010

*Merismopedia elegans A. Braun ex Kützing 110

Merismopedia insignis Skorbatow [Shkorbatow] 010

Microcystis wesenbergii (Komárek) Komárek ex Komárek 100

*Spirulina robusta H. Welsh 110

Chlorophyta

Desmodesmus abundans (Kirchmer) E. H. Hegewald 100

Monactinus simplex (Meyen) Corda 100

Pseudopediastrum boryanum (Turpin) E. Hegewald 100

Euglenophyta 

Lepocinclis acus (O. F. Müller) B. Marin & Melkonian 100

6Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e51160, enero-diciembre 2024 (Publicado Ago. 21, 2024)

Sites of sampling S1-ICO S2-MCH S3-IA

Salinity (PSU) mean values 0 PSU 32 PSU 25 PSU

Heterokontophyta (Bacillariophytina) 

Actinocyclus circellus T. P. Watkins 100

*Actinoptychus senarius (Ehrenberg) Ehrenberg 111

Actinoptychus splendens (Shadbolt) Ralfs 001

Alveus marinus (Grunow) Kaczmarska & Fryxell 011

Amphora proteus W. Gregory 010

*Asterionellopsis glacialis (Castracane) Round 101

Aulacoseira granulata (Ehrenberg) Simonsen 1 0 0

Azpeitia nodulifera (A. W. F. Schmidt) G. A. Fryxell & P. A. Sims 100

*Bacillaria paxillifera (O. F. Müller) T. Marsson 110

Bacteriastrum elongatum Cleve 011

Bacteriastrum furcatum Shadbolt 001

Bacteriastrum hyalinum Lauder 001

Sites of sampling S1-ICO S2-MCH S3-IA

Salinity (PSU) mean values 0 PSU 32 PSU 25 PSU

*Bellerochea malleus (Brightwell) Van Heurck 110

Biddulphia biddulphiana (J. E. Smith) Boyer 001

Biddulphia tridens (Ehrenberg) Ehrenberg 110

*Caloneis permagna (Bailey) Cleve 110

Campylodiscus braziliensis J. M. Deby 010

Cerataulus smithii Ralfs 001

Ceratoneis closterium Ehrenberg 001

Chaetoceros affinis Lauder 010

Chaetoceros brevis F. S chütt 010

Chaetoceros atlanticus Cleve 011

*Chaetoceros compressus Lauder 111

Chaetoceros curvisetus Cleve 011

Chaetoceros decipiens Cleve 011

Chaetoceros lorenzianus Grunow 011

Chaetoceros messanensis Castracane 110

Chaetoceros protuberans Lauder 001

Chaetoceros radicans F. S chütt 001

Chaetoceros rostratus Ralfs 001

*Cocconeis scutellum Ehrenberg 110

Coscinodiscus granii L. F. Gough 010

*Coscinodiscus radiatus Ehrenberg 111

Coscinodiscus rothii (Ehrenberg) Grunow 011

Coscinodiscus wailesii Gran & Angst 001

*Cyclotella stylorum Brightwell 111

*Cymbella tumida (Brébisson) Van Heurck 111

Detonula pumila (Castracane) Gran 011

*Diploneis bombus (Ehrenberg) Ehrenberg 111

Diploneis splendida Cleve 100

Ditylum brightwellii (T. West) Grunow 001

Sites of sampling S1-ICO S2-MCH S3-IA

Salinity (PSU) mean values 0 PSU 32 PSU 25 PSU

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e51160, enero-diciembre 2024 (Publicado Ago. 21, 2024)

Sites of sampling S1-ICO S2-MCH S3-IA

Salinity (PSU) mean values 0 PSU 32 PSU 25 PSU

*Entomoneis alata (Ehrenberg) Ehrenberg 111

Fragilaria sp. 100

*Grammatophora sp. 111

Grammatophora marina (Lyngbye) Kützing 010

*Guinardia delicatula (Cleve) Hasle 101

Guinardia flaccida (Castracane) H. Peragallo 001

*Gyrosigma inflatum Ricard 111

*Hantzschia pseudomarina Husted 111

Hantzschia sigma Hustedt 001

Haslea wawrikae (Husedt) Simonsen 010

Helicotheca tamesis (Shrubsole) M. Ricard 001

Hobaniella longicruris (Greville) P. A. Sims & D. M. Williams 001

*Hemiaulus sinensis Greville 111

Lauderia annulata Cleve 001

*Licmophora sp. 110

*Lithodesmium undulatum Ehrenberg 110

Lyrella lyra (Ehrenberg) Karajeva 010

Navicula sp. 100

Navicula gastrum (Ehrenberg) Kützing 010

Navicula lanceolata Ehrenberg 100

Navicula pennata A. W. F. Schmidt 011

Neidium sp. 010

*Nitzschia bicapitata Cleve 110

Nitzschia braarudii Hasle 001

Nitzschia granulata Grunow 011

*Nitzschia longissima (Brébisson ex Kützing) Grunow 111

Nitzschia sicula (Castracane) Hustedt 010

*Nitzschia sigma (Kützing) W. Smith 101

Nitzschia spathulata Brébisson ex W. Smith 001

Sites of sampling S1-ICO S2-MCH S3-IA

Salinity (PSU) mean values 0 PSU 32 PSU 25 PSU

Odontella aurita (Lyngbye) C. Agardh 011

Palmerina hardmaniana (Greville) G. R. Hasle 001

Petrodictyon gemma (Ehrenberg) D. G. Mann 100

Petroneis granulata D. G. Mann 010

*Pleurosigma angulatum (J. T. Quekett) W. Smith 110

*Pleurosigma diversestriatum F. Meister 111

*Podosira stelligera (Bailey) A. Mann 111

Proboscia alata (Brightwell) Sundström 001

Pseudo-nitzschia cf. pungens (Grunow ex Cleve) Hasle 001

Pseudo-nitzschia cf. pseudodelicatissima (Hasle) Hasle 001

Rhizosolenia setigera Brightwell 010

Rhopalodia sp. 010

Skeletonema sp. 100

Skeletonema costatum (Greville) Cleve 011

Stephanopyxis sp. 010

8Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e51160, enero-diciembre 2024 (Publicado Ago. 21, 2024)

Sites of sampling S1-ICO S2-MCH S3-IA

Salinity (PSU) mean values 0 PSU 32 PSU 25 PSU

*Surirella recedens A.W. F. Schmidt 111

*Surirella striatula Turpin 101

*Thalassionema bacillare (Heiden) Kolbe 110

Thalassionema nitzschioides (Grunow) Mereschkowsky 001

Thalassiosira lineoides Herzig & Fryxell 101

Thalassiosira delicatula Ostenfel 001

Thalassiothrix longissima Cleve & Grunow 001

Trieres mobiliensis (Bailey) Ashworth & E.C. Theriot 001

Dinoflagellata 

Azadinium cf. spinosum Elbrächter & Tillmann 001

*Blixaea quinquecornis (T. H. Abé) Gottschling 111

Cochlodinium sp. 001

Cochlodinium sp.1001

*Dinophysis fortii Pavillard 111

Sites of sampling S1-ICO S2-MCH S3-IA

Salinity (PSU) mean values 0 PSU 32 PSU 25 PSU

Diplopsalis sp. 001

Gonyaulax polygramma F. Ste in 010

Gonyaulax spinifera (Claparède & Lachmann) Diesing 011

Gonyaulax spirale Diesing 001

Gonyaulax sp. 010

Gyrodinium sp. 001

*Karenia mikimotoi (Miyake & Kominami ex Oda) Gert Hansen & Moestrup 101

Lingulodinium sp. 100

Peridinium quinquecorne var. trispiniferum Aké-Castillo & G. Vázquez 010

Protoperidinium abei (Paulsen) Balech 001

*Protoperidinium conicum (Gran) Balech 110

Protoperidium oceanicum (Vanhöffen) Balech 001

Protoperidium oviforme (P.J.L. Dangeard) Balech 001

Protoperidium ovum (J. Schiller) Balech 001

Protoperidinum pellucidum Bergh 001

Protoperidium pyriforme (Paulsen) Balech 001

Protoperidinium quarnerense (B. Schröder) Balech 001

Protoperidium subinerme (Paulsen) A. R. Loeblich III 001

*Prorocentrum gracile F. S chütt 110

*Prorocentrum micans Eh 101

*Tripos furca (Ehrenberg) F. Gómez 111

Tripos furca var. eugrammus (Ehrenberg) F. Gómez 0 1 0

*Tripos hircus (Schröder) F. Gómez 111

Scrippsiella trochoidea (F. Stein) A. R. Loeblich III 001

Scrippsiella spinifera G. Honsell & M. Cabrini 001

Warnowia sp. 001

∑ 53 64 79

S1-ICO: Station 1-Isla Conchas; S2-MCH: Station 2-Mandinga Chica, and S3-IA: Station 3-Isla del Amor. Practical Salinity

Unit (PSU): mean values, 1: Presence and 0: Absence. *Euryhaline taxa, and names of species in bold are new registers in

the area study

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e51160, enero-diciembre 2024 (Publicado Ago. 21, 2024)

Fig. 3. SEM A. Cerataulus smithii, external view showing ocelli and spines. B. Bacteriastrum hyalinum, Internal valve view

showing terminal setae. C. Lithodesmium undulatum, Valval view triangular, showing the central spine, each side having

a median inflation. D. Diploneis bombus, inside view cell showing rafe and striae. E. Azpeitia nodulifera, valve face with

radial rows of areolate. F. A. nodulifera, areolae occluded by criba and external aperture of rimoportula (arrow). Scale bars

F = 1 µm, D = 5 µm; A, B, C, E = 10 µm.

Fig. 2. Number of species by Phylum Heterokontophyta (Bacillariophytina), Dinoflagellata, Cyanobacteriota, Chlorophyta

and Euglenophyta registered in the Mandinga Lagoon.

10 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e51160, enero-diciembre 2024 (Publicado Ago. 21, 2024)

Table 3

Dominant species registered both in wet and dry seasons in the Mandinga Lagoon (2017-2018).

Taxa

ICOW17 MCHW17 ICOD18 MCHD18 IAD18 ICOW18 MCHW18 IAW18 Total

Bacillaria paxillifera 0 41 165 0 10 22 0 0 238

Chaetoceros compressus 0 0 42 19 147 0 0 0 208

Coscinodiscus rothii 0 0 29 7 20 24 22 29 132

Chaetoceros atlanticus 0 0 30 17 23 20 37 0 127

Merismopedia elegans 10 0 0 98 0 0 0 0 108

Nitzschia bicapitata 72 28 0 0 0 0 0 0 100

Skeletonema costatum 0 39 11 0 0 0 0 49 99

Gyrosigma inflatum 0 24 6 15 5 18 17 0 85

Blixaea quinquecornis 54 0 16 0 10 0 0 0 80

Navicula pennata 53 0 8 8 0 0 0 0 69

∑ 188 132 307 163 214 83 76 79

Data expressed in 103 cells/ml. ICOW17: Isla Conchas Wet 2017; MCHW17: Mandinga Chica Wet 2017; ICOD18: Isla

Conchas Dry 2018; MCHD18: Mandinga Chica Dry 2018; IA18: Isla del Amor Dry 2018; ICOW: Isla Conchas Wet/Rainfall

2018; MCHW: Mandinga Chica Wet 2018 and IAW18: Isla del Amor Wet 2018.

Phytoplankton composition: A total of

136 taxa distributed in five Phylum were regis-

tered, 68.4 % (93) to Heterokontophyta (Baci-

llariophytina), 22.8 % (31) to Dinoflagellata, 5.9

% (8) of which correspond to Cyanobacteria,

2.2 %, (3) to Chlorophyta, and 0.7 % (1) to

Euglenophyta (Fig. 2 and Fig. 3).

Abundance phytoplankton: Heterokon-

tophyta species rank eight places out of the first

10 in abundance: B. paxillifera, C. compressus,

C. rothii, C. atlanticus, N. bicapitata, S. costa-

tum, G. inflatum, and N. pennata. To complete

the list one Cyanobacteria: M. elegans, and one

Dinoflagellata: B. quinquecornis. Regarding the

stations and seasons studied, the highest abun-

dance was 307 x 103 cells/ml during the dry

season in the ICO station in 2018; instead, the

lowest abundance was observed in the MCH

station during the wet season in 2018 with 76 x

103 cells/ml (Table 3).

Diversity Index and species dominance:

The Shannon index showed a maximum value

of 1.31 bits/ind. at ICO in the dry season

(2018), the minimum value was 0.70 bits/ind.

in IA during the wet season (2018).

According to the Olmstead-Tukey diagram,

the dominant groups were Heterokontophyta

and Dinoflagellata; 48 % of the phycoflora were

rare species, followed by 29 % dominants, 20 %

constant, and 3 % occasional—some examples

of the dominant: B. paxillifera, C. compressus,

C. rothii, and C. atlanticus. In contrast, the con-

stant was G. marina. Moreover, the occasional

was D. abundans. Lastly, A. proteus was rare

(Fig. 4).

Analysis of phytoplankton and limnolog-

ical variables: Our results show that quadrant

I was related to salinity and dissolved oxygen

with C. rothii and C. closterium (Heterokon-

tophyta). The quadrant III was associated with

phosphates, whose taxa were represented by B.

paxillifera, C. atlanticus, P. stelligera, A. senari-

us, and B. quinquecornis (Dinoflagellata). The

quadrant IV was related to pH, nitrates and

temperature; the highest water temperature val-

ues, 27-29 °C, with T. furca, T. hircus, P. m ic a n s ,

C. curvisetus, and M. elegans (Cyanobacteria).

At the same time, the species of quadrant II did

not show a relation with limnological variables,

e.g. S. costatum, C. scutellum, and N. bicapitata

(Fig. 5).

DISCUSSION

Limnological variables: The variables

showed the following based on the data

obtained during 2017-2018 (Table 1). The

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e51160, enero-diciembre 2024 (Publicado Ago. 21, 2024)

Fig. 4. Olmstead-Tukey diagram showing the importance of species: dominant, occasional, constant and rare from Mandinga

Lagoon.

Fig. 5. Canonical Correspondence Analysis. The relationship between species and environmental variables studied from

Mandinga Lagoon. The axes explain 56 % of total variance.

12 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e51160, enero-diciembre 2024 (Publicado Ago. 21, 2024)

surface temperature of the water ranged from

27-29 °C in the dry season, while in the wet sea-

son, it ranged from 21-22 °C. For this reason,

during the dry season, water temperature falls

into the classification of tropical environments,

according to Lara-Domínguez et al. (2011) for

several lagoons in Veracruz.

In contrast, data from 1975 by Arreguín-

Sánchez (1982) indicated temperatures from

16 to 32 °C, with the lowest temperatures

during January and February. Also, Salcedo-

Garduño et al. (2016) and Salcedo-Garduño

et al. (2019) showed temperature registrations

from 20.8 to 29.9 °C, as well as temperatures

from 28 to 31 °C in the dry season and rains

in the same lagoon by González-Vázquez et

al. (2019). There also similar temperature reg-

istrations from 23 to 33 °C for the Alvarado

Lagoon (Rivera-Guzmán et al., 2014) and from

22.8 to 26.2 °C in Sontecomapan (Muciño-

Márquez et al., 2012).

For the study area, the average pH value

was 8.3 ± 0.26, while the minimum was 8 in

the wet season; these are slightly basic chemi-

cal conditions due to the influence of seawater

intrusion into the coastal lagoons. For other

habitats of Veracruz, such as the Tapamachoco

Lagoon, Contreras & Warner (2004) indicate a

pH of 8.0-8.2. While for the winters, the regis-

tered pH was 7.1-7.8, which can be explained

by the degradation of organic matter or by

removing sediment due to the effects of the cur-

rent, causing remineralization (López-Ortega

et al., 2012). Also, for the La Mancha Lagoon,

the pH in the dry season is 7.8 and rainy is 8.1

respectively (Rivera-Guzmán et al., 2014). At

Sotecomapan Lagoon value was near neutral,

7.3-7.8 (Muciño-Márquez et al., 2012).

The salinity in this study ranged between

0 to 32 PSU, which is why it is considered an

euryhaline environment. Therefore, it is not

confirmed as polyhaline (10-20 PSU) as indi-

cated by Lara-Domínguez et al. (2011), Salcedo-

Garduño et al. (2016) and Salcedo-Garduño et

al. (2019), whose values ranged between 21-31

PSU. Likewise, Arreguín-Sánchez (1982) and

González-Vázquez et al. (2019) recorded in

Mandinga Lagoon values of 0.5 to 33 PSU

during dry and wet seasons. These data should

not be forgotten that they can be very dynamic

due to the change of tides, such as that recorded

in the Sontecomapan Lagoon, Veracruz, during

the nyctemeral cycle in the rainy season where

the change of tides explains the values 3 to 6

PSU in the morning while 30.5 PSU later at 5:00

P.M. (Muciño-Márquez et al., 2012).

The values for dissolved oxygen ranged

from 6.7 to 9.3 mg/L, which is why this envi-

ronment is recognized as well-oxygenated

(Salcedo-Garduño et al., 2016). These data

confirm what was stated by Lara-Domínguez

et al. (2011) for the coastal lagoons of the Gulf

of Mexico, where the efficient pattern of water

circulation and renewal, as well as an intense

activity of primary producers, allow a dynamic

of this limnological condition in a well-oxygen-

ated coastal environment.

Our nitrate and phosphate values for Man-

dinga Lagoon ranged from 0 to 1 mg/L and 0 to

2.2 mg/L, respectively. The highest values were

initially recorded in the wet season, explained

by the nutrient incorporation and dragging

into the basin. Instead, Salcedo-Garduño et

al. (2016) indicated concentrations of nitrates

from 0.15 to 0.6 mg/L and phosphates from

0.08 to 0.15 mg/L from 2011 to 2012. For its

part, Contreras-Espinosa et al. (1994) indicated

that nitrates from 33 Mexican coastal lagoons

ranged from 0.049 to 0.070 mg/L and support-

ed the idea that these nutrients are generally

higher in the wet season. These values do not

correspond to the nutrient ranges found in the

coastal lagoons of Veracruz, where the number

of nitrates ranged from 0.05 to 0.14 mg/L and

the number of phosphates from 0 to 0.15 mg/L

(Lara-Domínguez et al., 2011). Vázquez et al.

(2007) mainly report nitrate amounts of 1.6, 1.1,

and 1.4 mg/L and phosphorus amounts of 0.9,

1.5, and 1.8 mg/L for eutrophic lakes Chalchoa-

pan, Verde, and Mogo, Veracruz, respectively.

During the study period in Mandinga

Lagoon, the chlorophyll-a levels ranged from 3

to 11 mg/m3, implying low primary productivity

in the system. Contreras-Espinosa et al. (1994)

and Lara-Domínguez et al. (2011) recorded

values from 30 to 40 mg/m³ during the same

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e51160, enero-diciembre 2024 (Publicado Ago. 21, 2024)

seasons, which indicates that the registration

was higher at another season. Also, Salcedo-

Garduño et al. (2019) indicated values from 8 to

15 mg/m3 in the same climatic seasons. On the

other hand, in Tampamachoco Lagoon, values

from 10 to 20 mg/m³ were recorded in 1980; a

decade later, the records were 20 to 30 mg/m³,

which indicates that there are changes in limno-

logical dynamics over time, associated with the

abundance of photosynthetic organisms that, in

turn, are responsible for the dissolved oxygen

concentrations reached in the water column.

During the wet season, the maximum con-

centration of chlorophyll-a, Secchi transpar-

ency, and lower phytoplankton abundance was

observed compared to the dry season (Table 1).

These differences in chlorophyll-a and abun-

dances could be because, in this work, the

picoplankton photosynthetics were not quanti-

fied in both periods, whose lighting and mixing

variables in the water column contributed to

these differences.

Phytoplankton composition: In this study,

136 taxa were found, 68.4 % Heterokontophyta,

followed by 22.8 % Dinoflagellata (Table 2);

such composition is typical of euryhaline envi-

ronments. That is, diatom and dinoflagellate

dominance are similar to that registered in

brackish aquatic Dzilam, Tamiahua and Man-

dinga Lagoons from Yucatan and Veracruz,

Mexico (Figueroa-Torres & Weiss-Martínez,

1999; Herrera-Silveira et al., 1999; Salcedo-

Garduño et al., 2019).

Of the total phycoflora, the following Phy-

lum are cited for the first time: Cyanobacteria,

Euglenophyta, and Chlorophyta; in the last

Phylum, the Pseudopediastrum can grow in

an oligohaline habitat whose salinity intervals

range from 0 to 10 PSU. This genus is one

of the typical phytoplankton components of

a polyhaline environment such as Tamiahua

Lagoon, where salinities are from 18 to 30 PSU

(Figueroa-Torres & Weiss-Martínez, 1999).

Otherwise, from the composition of the dia-

toms indicated by Barón-Campis et al. (2005),

the presence of six genera Chaetoceros, Navicu-

la, Pleurosigma, Pseudo-nitzschia, Skeletonema,

and Thalassionema was confirmed, during the

study, while the genus Lioloma was not record-

ed in this work.

The specific phytoplankton richness reg-

istered in Mandinga Lagoon can be rated as

high, as opposed to what was indicated for

other coastal lagoons in the Gulf of Mexico,

such as Tamiahua with 39 species of Dinoflagel-

lata (Figueroa-Torres & Weiss-Martínez, 1999),

Alvarado with 18 species (Margalef, 1975), and

Lagartos with 67 species (Nava-Ruíz & Valadez,

2012). We recognized 93 species of diatoms, of

which the genera with the highest species rich-

ness were Chaetoceros with eleven and Nitzschia

with seven. Krayesky et al. (2009) indicate simi-

lar data for the Southwestern Gulf of Mexico,

where both genera present the highest richness

with 27 and 16 species, respectively.

Pseudo-nitzschia species in the study area

can warn about the need for surveillance as

they are HAB-causing agents (Salcedo-Gardu-

ño et al., 2019). Regarding the Dinoflagellata,

the studied stations registered 31 species, cor-

responding to 12 % of that indicated for the

Southwest of the Gulf of Mexico (Steidinger

et al., 2009), where the genus with the highest

number of species was Protoperidinium with

nine species. This taxon was mainly associ-

ated with the IA station, the closest area to the

system’s mouth. Therefore, many of its com-

ponents are typically marine, where 25 PSU

were registered, conditions consistent with the

high diversity of species defined by Okolodkov

(2008) for the marine coasts of Veracruz, where

46 species of that genus were found. In three

stations studied, B. quinquecornis was found in

low 80 x 103 cells/ml concentrations. This spe-

cies has been associated with HAB in the port

of Veracruz (Barón-Campis et al., 2005), for

which it is highly recommended to monitor the

dynamics of this population to prevent future

environmental contingencies in the study area.

For the Cyanobacteria, eight species were

found only at the ICO and MCH stations, and

M. elegans, M. insignis, and M. wesenbergii were

registered for the first time. These taxa corre-

spond to 18 % of those listed for the Southwest

of the Gulf of Mexico (León-Tejera et al., 2009).

14 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e51160, enero-diciembre 2024 (Publicado Ago. 21, 2024)

Abundance phytoplankton: Out of the

ten abundant species in the study area, the

maximum quantification corresponded to the

2018 period in the ICO station, with 307 x

103 cells/ml in the dry season. In contrast, the

minimum concentration was 76 x 103 cells/ml

in the MCH station in the wet season (Table 3).

High amounts of productivity, if we compare

them with the records of 4 x 103 cells/ml in the

rainy and windy seasons at Alvarado’s Lagoon

indicated by Margalef (1975). Therefore, both

lagoons record minimum phytoplankton con-

centrations in the rainy season. This suggests a

variation in the quantification of phytoplank-

ton, which showed a higher record in the dry

season when the depth of the Secchi disk was

43 cm, where the picoplankton could be essen-

tial components of chlorophyll production in

the system. The support mentioned above was

indicated by Kjerfve & Magill (1989); they say

that, during the wet seasons, cyclone, hurri-

cane, tropical storm, and waterspout seasons

are associated, which produce changes in the

ecosystem and its components, e.g., salinity,

nutrients, winds, and the deposition of fresh-

water by the tributaries. For that reason, the

phytoplankton cannot grow appropriately.

Instead, during the dry season, where con-

ditions remain similar, some components of

the phytoplankton can grow exponentially. The

species with the highest abundance in the study

area was B. paxillifera.

According to Jahn & Schmid (2007), this

diatom, a ubiquitous taxon, has been recorded

worldwide in freshwater, brackish, and marine

habitats. Despite the changes in limnological

conditions, these species do not experience

growth limitations. Likewise, this species has

also been indicated as an abundant component

of 39 x 103 cells/L from Sontecomapan Lagoon,

Veracruz (Muciño-Márquez et al., 2012).

Species dominance: Our results showed a

phytoplankton composition mainly made up of

diatoms and dinoflagellates in 91.6 %. This is

consistent with some authors’ statements that

Bacillariophyta and Dinoflagellata account for

approximately 80 % of the eukaryotic species

of marine phytoplankton (Licea et al., 2004;

Licea et al., 2011; Muciño-Márquez et al., 2014).

As well as the presence of Alveus marinus,

Chaetoceros atlanticus, C. lorenzianus, D. bom-

bus, N. pennata, N. granulata, N. longissima, S.

costatum, Gonyaulax spinifera, Dinophysis fortii,

Pseudo-nitzschia cf. pseudelicatissima, and P. cf.

pungens, among others. This indicates seawater

intrusion into the lagoon by tidal currents or

wind, consistent with what was stated in stud-

ies for different coastal lagoons. As opposed to

Lagartos Lagoon, Quintana Roo, more than 80

% of its phytoplankton comprises Cyanobacte-

ria, which suggests that the system is eutrophi-

cated (Nava-Ruíz & Valadez, 2012).

The highest Shannon-Wiener index in this

study was 1.31 bits/ind., indicating some spe-

cies’ high dominance and low equity. These

results are lower than the one cited for the

Palizada del Este Lagoon, Campeche-Mexico;

there was an index of 3.2 bits/ind. (Muciño-

Márquez et al., 2014). Also, in a marine region

near Punta Limón, Veracruz, the data were from

1.9 to 4.1 bits/ind. (Santoyo & Signoret, 1988).

Relationship between phytoplankton

and limnological variables: Some species of

the abundant genera in this study, includ-

ing Chaetoceros, Grammatophora, Gyrosigma,

and Nitzschia (Table 2 and Table 3), have

been used as indicators of salinity in previous

studies and are associated with wide tempera-

ture ranges, which gives them the category of

salinity eurythermal and euryhaline (Rivera-

Guzmán et al., 2014).

Phosphates and salinity (zero) explain the

presence of Chlorophyta species in the wet

season at ICO (Table 2). This would be relevant

for the variables indicated, as well as for the

environmental conditions recorded, for exam-

ple, some species of Pediastrum sensu lato for

Central Europe and Mexico (Lenarczyk, 2015;

Garduño et al., 2016).

On the other hand, nitrates, water temper-

ature, and pH explain the presence of dinofla-

gellates in the dry season in ICO and IA. These

results have also been recorded in the Celes-

tun Lagoon, Yucatan, where dinoflagellates

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e51160, enero-diciembre 2024 (Publicado Ago. 21, 2024)

withstand wide temperature ranges (Herrera-

Silveira et al., 1999). This group shows a cor-

relation between temperature and abundance,

which is consistent with the results obtained

in this study. However, it should be noted that

some species of the genera Ceratium, Prorocen-

trum, and Gyrodinium can tolerate salinities

from 10 to 70 PSU (Taylor, 1978). In general,

the limnological variable and the phytoplank-

ton diversity show temporality, which reflects

variations in the environment and the activities

of human populations that depend directly or

indirectly on the lagoon water, precipitation

and deposition of the tributaries mainly. Sal-

cedo-Garduño et al. (2019) indicated a shallow

environment for Mandinga Lagoon with the

influence of marine and continental water from

the Jamapa River. They also report a more sig-

nificant variability in the phytoplankton abun-

dance during the wet season.

Ethical statement: the authors declare that

they all agree with this publication and made

significant contributions; that there is no con-

flict of interest of any kind; and that we fol-

lowed all pertinent ethical and legal procedures

and requirements. All financial sources are fully

and clearly stated in the acknowledgments sec-

tion. A signed document has been filed in the

journal archives.

ACKNOWLEDGMENT

We would like to thank all colleagues who

helped us work SEM Rafael Quitanar Zuñiga

and pictures Daniel Sánchez Ávila. Finally,

the anonymous reviewers added their valuable

comments to the final writing.

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